Tag Archives: host alternation

This year has been a bit of a bumper PhD submission year for me, five of my PhD students have come to the end of their time, and have submitted, or will soon be submitting their theses. In my experience, 48 successful students and counting, it is relatively easy to reassure PhD students that their worries about the structure of their thesis, the appropriateness of their analysis and how many tables and figures they should have, are not justified. Many of them already have papers in print or in press by the writing-up stage so they only need a little bit of reassurance about the quality of their work. The bit that seems to worry them most is the General Discussion. My advice to them was, and is, the same as that given to me by my supervisor 37 years ago, “spread your wings, sell your work, don’t be afraid to speculate a little, enjoy yourself and make sure you don’t just summarise your thesis”.

This uncertainty about how to handle the General Discussion is not just a foible of my students. My impression over the last few years, borne out by the increasing frequency on which I comment on the shortcomings of the General Discussion of the PhD theses that I examine (now more than sixty) is that General Discussions are not what they used to be. I too often find myself reading a series of lightly edited chapter abstracts, which in my opinion is not a General Discussion. Am I, however, suffering from grumpy old git syndrome or were General Discussions more general in the days of my youth? How for example, does my General Discussion stack up compared with that of the modern-day PhD student? Did I practice what I now preach?

I do of course still have a copy of my thesis (Leather, 1980), two to be precise. Both my parents were biologists, albeit botanists, so I felt obliged to give them a copy, which I retrieved when clearing my Mother’s house after her death. The upshot being that I have no excuse for not being able to find a copy from which to do a critical appraisal of my General Discussion. My thesis was written before Word Processors existed, and when computers occupied their own buildings. It was typewritten (by me using a Silver Reed A3 typewriter) and so no electronic copies are available. As a consequence, I have had to scan the parts relevant to my story; hence the poor quality of the illustrations 🙂

At this point, I should point out that although I was trained as an agricultural entomologist and my PhD was about an agricultural pest, the bird cherry-oat aphid, my supervisor, Tony Dixon, was and still is, an ecologist. Our lab was thus a mixture of pure and applied ecologists, some of whom weren’t even entomologists 🙂 This meant that I was exposed to a wider range of ideas than if I had just been in a lab of only applied entomologists. Despite not being overly mathematical or theoretically inclined, I’m pretty much an empirical ecologist (field and lab), I was very impressed by the late, great E.C. Pielou, to the extent that I bought her book Ecological Diversity and read it cover to cover*. Working with a host alternating aphid, I immediately latched on to her definition of seasonality as being synonymous with environmental variability (Pielou, 1975) and decided to coin a new term, seasonability** .

An excellent start, the title page doesn’t even mention the words General Discussion 🙂

I defined seasonability as being “the pre-programmed response to predictable environmental change” in my terms this meant that the organism, in this case my aphid, anticipates the trend in conditions, something I, and a more mathematically inclined colleague did actually show a couple of years later (Ward et al., 1984). I then drew the analogy that an aphid clone could be equated with Harper’s visualisation of a plant being constructed of a series of genetically identical modular units (Harper, 1977), i.e. each individual within the clone, although being genetically identical has a specific (and seasonal) function I also managed to slip in a reference to my other ecological hero, Dan Janzen at this point (Janzen, 1977) 🙂

I see that I was keen to introduce new terms, as my second figure shows. I was amused to see in figure legend that I describe the x-axis as food quality but label it as host quality in the

A pretty lousy figure, but remember we had to draw our figures by hand in those days. Here I attempt to coin another new usage, this time refluence, to indicate the flowing back of the clone to the primary host.

figure, doing something that in later years I have waxed wrathfully against (Leather & Awmack, 1998; Awmack & Leather, 2002). In this case, food (nutritional) quality is the term I should have used although I could argue that the build-up of natural enemies on the secondary grassy hosts and the predictable absence of natural enemies on the primary host, could justify the use of the term host quality, but that would be post hoc sophistry and best avoided 🙂

I was obviously also very keen to introduce new meanings to words as my third figure shows.

Yet another attempt to coin a new meaning for an existing word

At no point however, did I summarise what was in each chapter. I referred in passing to one…”It is now fairly certain from the evidence presented on the effects of growth stage (Chapter 4) that..” and the four figures are unique to my General Discussion, even the two that contained data points, so I can pat myself on the back in that respect. Although I did not extend my discussion to other taxa, I did range far and wide across the aphid world so I think that fulfilled the brief of spreading my wings, and boy did I try and sell my work.

I also notice that the 25-year-old me tried very hard to use a different sort of language in his General Discussion such as, “lends further credence to the concept of seasonability” which is followed in the next sentence by “..when the bursting of the buds of the tree host or resurgence of sap in the perennial herbaceous host, heraldthe start of egg hatch”. Yes, I actually used the word herald, but then, this is the guy who prefaced his thesis with these two quotes.

The Steinbeck quote (Doc from Sweet Thursday, does still sums up pretty much what I want to do with my life.

So what does the 62-year-old Professor of Entomology think about the efforts of his younger self? I may be slightly biased, but I think it is a reasonable effort and as an examiner I wouldn’t have any major problems with it although I suspect that I would be tempted to have a gentle dig at the attempts to coin new terms. Overall I would rate it as B+.

In case you wondered , although I never published, or even tried to publish my General Discussion, all the ideas, except for the terms which were petty awful, (or naff as we would say in the UK), have made it into print at some time.

To reiterate, my advice to PhD students struggling with your General Discussion is “spread your wings, be bold, sell your work, don’t be afraid to speculate a little, enjoy yourself and most importantly, definitely make sure you don’t just summarise your thesis”

I have written before about aphids and how their quest for the ideal food plant may explain the evolution of host alternation; we find that most aphid species tend to be associated with rapidly growing meristems, or newly flushing leaves (Dixon, 2005). Some aphids are so keen on young plant tissue that they ‘engineer’ youth in their host plants, injecting salivary compounds and forming leaf–rolls, pseudo-galls and galls, all of which act as nutrient sinks and lengthen the time that the modified leaves stay green and nutrient-rich

Non host-alternating (autoecious) aphids, such as the sycamore aphid Drepanosiphum platanoidis, the maple aphid, Periphyllus testudinaceus, or the birch aphid, Euceraphis punctipennis, have no such escape route; they are confined to their tree host for the year, albeit, they can, if they ‘wish’, fly to another tree of the same species, but essentially they are held hostage by the their host plant. As the season progresses, leaf nutritional and physical properties change; going from young tender green leaves, with high nitrogen and water contents, to mature, tough leaves, low in nitrogen and water to yellow senescing leaves with again, higher nitrogen levels (Awmack & Leather, 2002) and finally of course, dead brown leaves of no nutritional value.

Sycamore and maple aphids, enter a state of suspended animation ‘summer aestivation’ (Essig, 1952; Dixon, 1963), whilst birch and poplar aphids, whose hosts plants often produce new growth during the year, ‘track’ these new leaves (Wratten, 1974; Gould et al., 2007). As far as these aphids are concerned young tissue is their best food source, with senescent tissue being second best and mature leaves being least favoured. During the summer they will, however, take advantage of mature leaves that are prematurely senescing, such as those attacked by leaf diseases such as tar spot. I have often found sycamore aphids feeding and reproducing on these infected leaves whilst those aphids on neighbouring mature leaves remain in aestivation.

Effects of tar spot on sycamore leaves

Host-alternating (heteroecious) aphids on the other hand are somewhat different. As their life cycle includes a programmed migration back to their primary tree host in autumn, those autumn morphs (oviparae) are adapted to senescent tissue (Leather & Dixon, 1982, Kundu & Dixon, 1993, 1994). Similarly, the spring morphs (fundatrices and fundatrigeniae) are adapted to young leaves and find it difficult or impossible, to make a living on senescent leaves.

There are yet other aphids, such as the green spruce aphid Elatobium abietinum, the pine aphid, Eulachnus agilis and the black pecan aphid, Melanocallis caryaefoliae, that are senescence specialists. In contrast to the flush specialists, these aphids engineer senescence, also using salivary compounds, and are unable to survive on young foliage (Bliss, 1973; Fisher, 1987; Cottrell et al., 2009).

It is interesting to speculate that perhaps these tree-dwelling non host-alternating aphids are secondarily derived from the autumn part of the life-cycle of host-alternating aphids. After all, if non host-alternating aphids on herbaceous host plants are off-shoots of the summer part of the host-alternating life-cycle why not the other way round. There is just so much more to learn about aphids. Yet another reason why I love aphids so much 😉

A lot of what I describe comes from a talk I gave in 2009 at a workshop in Oxford on autumn colours (the output of which was Archetti, M., Döring, T.F., Hagen, S.B., Hughes, N.M., Leather, S.R., Lee, D.W., Lev-Yadun, S., Manetas, Y., Ougham, H.J., Schaberg, P.G., & Thomas, H. (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends in Ecology & Evolution, 24, 166-173. I always meant to write the talk up as an Opinion piece but procrastination set in badly. I was somewhat annoyed with myself when earlier this year this excellent piece by the legendary ecologist and entomologist, Tom White, appeared; I have only myself to blame, six years is a very long bit of procrastination 😉

This post is dedicated to my eldest son, Sam, who died quietly in his sleep, at a tragically young age, December 23rd 2010. It would have been his birthday on the 21st May. Despite being a molecular biologist, (he worked at the Sanger Institute), he was as green as you can get, a great naturalist and conservationist, with an incredibly gentle soul. He strongly believed in conserving the World’s natural resources and amused colleagues by sticking up signs in the toilets at the Sanger, which read “If its yellow let it mellow, if its brown flush it down”.

He is sorely missed by us all. He also had more Nature papers than me 😉

In a very early post I mentioned that one of the reasons that I love aphids so much is their life-cycles https://simonleather.wordpress.com/aphidology/ and the fantastic jargon that is used to describe them. Many undergraduates find the jargon off-putting but it was this complexity that really grabbed my imagination.

Insects are probably the most diverse group of organisms on Earth (Grimaldi & Engel, 2005) and their life cycles range from simple sexual and asexual styles to complex life cycles encompassing obligate and facultative alternation of sexual and asexual components. Nancy Moran (1992) suggests that in the insect world probably the most intricate and varied life cycles are found in aphids and I certainly wouldn’t disagree.

There are basically two types of aphid life-cycles, non-host alternating (autoecious, monoecious) and host alternating (heteroecious). Autoecious aphids spend their entire life cycle in association with one plant species as shown below (Dixon, 1985).

(or group of related plant species), whereas heteroecious aphids divide their time between two very different species of host plant, usually a tree species (the primary host) on which they overwinter, and an herbaceous plant species (the secondary host) on which they spend their summer.

Approximately 10% of aphid species are heteroecious. The ancestral aphid life cycle is thought to have been winged, egg laying and autoecious on a woody host plant almost certainly conifers and the oldest families of woody angiosperms e.g. Salicaceae (Mordwilko, 1928; Moran, 1992).

Aphid life cycles can also be described as holocyclic, in which cyclical parthenogenesis occurs, with aphids reproducing sexually in the autumn to produce an overwintering egg, in temperate regions and parthenogenetically during spring and summer as shown below for the sycamore aphid (Dixon, 1985).

Some aphids are anholocyclic where the clone is entirely asexual reproducing by parthenogenesis throughout the year. This is often seen in locations where winter conditions are mild, in the tropics for example or as a bit of an oddity around hot-springs in Iceland.

Parthenogenesis in aphids is coupled with live births and reduced generation times through the phenomenon of telescoping generations. Parthenogenesis in aphids developed early on but whether the oldest aphids (200 mya) were parthenogenetic is not known.

Host alternation appears to have arisen more than once (Moran, 1988) and occurs in four slightly different forms depending on the taxon in which it occurs. The main differences being in whether the sexual forms are produced on the primary (winter) host (the host on which the eggs are laid), or as in the case of the Aphidini, the males being produced on the secondary (summer) host and the sexual females produced on the primary host. The majority of aphids host alternate between unrelated woody and perennial hosts, but some species host alternate between herbaceous plants e.g. pea aphid Acyrthosiphon pisum alternates between the perennial vetches and the annual peas Pisum sativum (Muller & Steiner, 1985) and Urleucon gravicorne alternates between the perennial Solidago and the annual Erigeron (Moran 1983). Some aphid species such as Rhopalosipum padi, have clones that are holocyclic and some that are anholocyclic, so hedge their bets and also gives me the opportunity to slip in a great slide kindly lent to me by my friend Richard Harrington at Rothamsted Research.

One of the things that is rather puzzling is why some aphid species should have adopted a host alternating life cycle which on the face of it, seems to be rather a risky strategy. You could liken it to looking for a needle in a hay-stack; only about 1 in 300 aphids that leave the secondary host at the end of summer are likely to find their primary host (Ward et al, 1998). There are a number of theories as to why it has evolved.

1. The nutritional optimization through complementary host growth hypothesis states that heteroecy has been favoured by natural selection because it enables a high rate of nutrient intake throughout the season (Davidson, 1927; Dixon, 1971). In essence, the clone moves from a host plant where food quality is low and moves onto a herbaceous host that is growing rapidly and thus provides a good source of nutrition. In autumn, the clone moves back to its primary woody host where leaves are beginning to senesce and provide a better source of nutrition as seen below (Dixon, 1985).

On the other hand, non-host alternating aphids such as the sycamore aphid, Drepanosiphum platanoidis, or the maple aphid, Periphyllus testudinaceus, reduce their metabolism and tough it out over the summer months when the leaves of their tree hosts are nutritionally poor, the former as adults, the latter as nymphs (aphid immature forms) known as dimorphs. Mortality over the summer in these species is, however, very high. In some years I have recorded almost 100% mortality on some of my study trees, so very similar to the 99.4% mortality seen in the autumn migrants (gynoparae) of the bird cherry-oat aphid, Rhoaplosiphum padi. Other autoecious aphids are able to track resources if they live on host plants that continue to develop growing points throughout the summer.

Verdict: No apparent advantage gained

2. The oviposition site advantage hypothesis states that primary woody hosts provide better egg laying sites and provide emerging spring aphids with guaranteed food source (Moran, 1983). There is however, no evidence that eggs laid on woody hosts survive the winter better than those laid in the herbaceous layer. Egg mortality in both situations ranges from 70-90% (Leather, 1983, 1992, 1993).

Verdict: No apparent advantage gained

3. The enemy escape hypothesis states that by leaving the primary host as natural enemy populations begin to build up and moving to a secondary host largely devoid of enemies confers an advantage on those species that exhibit this trait (Way & Banks, 1968). At the end of summer, when the natural enemies have ‘found’ the clone again, the clone then migrates back to its primary host, which theoretically is now free of natural enemies. This is an attractive idea as it is well known that natural enemies tend to lag behind the populations of their prey.

Verdict: Possible advantage gained

4. The Rendez-vous hosts hypothesis suggests that host alternation assists mate location and enables wider mixing of genes than autoecy (Ward, 1991; Ward et al. 1998). This seems reasonable, but as far as I know, no-one has as yet demonstrated that host-alternating aphid species have a more diverse set of genotypes than non-host alternating aphids.

Verdict: Not proven

5. The temperature tolerance constraints hypothesis which postulates that seasonal morphs are adapted to lower or higher temperatures and that they are unable to exist on the respective host plants at the ‘wrong time of year’ (Dixon, 1985). I don’t actually buy this one at all, as I have reared spring and autumn morphs at atypical temperatures and they have done perfectly well (Leather & Dixon, 1981), the constraint being the phenological stage of their host plant rather than the temperature. In addition, there are some host alternating aphid species in which the fundatrix can exist on both the secondary and primary hosts (if the eggs are placed on the secondary host). This has been experimentally demonstrated in the following species:

6. The escape from induced host-plant defences hypothesis (Williams & Whitham, 1986), which states that by leaving the primary host as summer approaches, the aphids escape the plant defences being mustered against them. This is only really applicable to those gall aphids where galled leaves are dropped prematurely by the host plant.

Verdict: Special case pleading?

7. The constraint of fundatrix specialisation hypothesis is that of Moran (1988), who argues that heteroecy is not an optimal life cycle but that it exists because the fundatrix generation (the first generation that hatches from the egg in spring) on the ancestral winter host, are constrained by their host affinities and are unable to shift to newly available nutritionally superior hosts. Whilst it is true that some host alternating aphids are however, very host specific as fundatrcies, some aphids are equally host-specific as oviparae at the end of the year the constraints of ovipara specialisation

For example, in the bird cherry-oat aphid Rhopalosiophum padi, the fundatrices are unable to feed on senescent leaf tissue of the primary host, their offspring can only develop very slowly on ungalled tissue and all their offspring are winged emigrants (the alate morph that flies from the primary host to the secondary host) (Leather & Dixon, 1981). The emigrants are able to feed as nymphs on the primary host on which they develop and as adults on their secondary host, but not vice versa (Leather et al., 1983). The autumn remigrants (gynoparae, the winged parthenogenetic females that fly from the secondary hosts to the primary hosts on the other hand, feed on the secondary host as nymphs but are unable to feed on the primary host as adults (Leather, 1982; Walters et al., 1984). The black bean aphid shows similar, but less rigid host specificity and whilst there is a distinct preference for the relevant host plant (Hardie et al., 1989), parthenogenetic forms can occur throughout the summer on the primary host (Way & Banks, 1968), particularly if new growth is stimulated by pruning (Dixon & Dharma, 1980). There are also at least two examples of where both the primary and secondary host are herbaceous (see earlier). In both these cases the fundatrices could exist on both the primary and secondary host plants

Verdict: Not proven

So what do I think? For years I was very firmly convinced that the nutritional optimization hypothesis was the obvious answer; after all Tony Dixon was my PhD supervisor 😉 Now, however, having lectured on the subject to several cohorts of students, if I was forced to pick a favourite from the list above, I would do a bit of fence-sitting and suggest a combination of the nutritional optimization and enemy escape hypotheses. What do you think? There are cetainly a number of possible research projects that would be interesting to follow up, the problem is finding the funding 😦

Sources

Blackman, R.L. & Devonshire, A.L. (1978) Further studies on the genetics of the carboxylase-esterase regulatory system involved in resistance to orgaophosphorous insecticides in Myzus persicae (Sulzer). Pesticide Science 9, 517-521

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